Regulation of 3-Hydroxy-3-Methylglutaryl-CoA Synthase and 3-Hydroxy-3-Methylglutaryl-CoA Reductase and Rubber Biosynthesis of Hevea brasiliensis (B.H.K.) Mull. Arg

  • Pluang Suwanmanee
  • Nualpun Sirinupong
  • Wallie Suvachittanont
Chapter

Abstract

It is rather well established that rubber biosynthesis in rubber trees (Hevea brasiliensis) takes place in laticifers and is dependent on mevalonate (MVA). 3-Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR, EC 1.1.1.34) has been shown to catalyze a rate-limiting step in this pathway. However, our studies demonstrated that both 3-hydroxy-3-methylglutaryl coenzyme A synthase (HMGS, EC 2.3.3.10) and HMGR are essential enzymes involved in rubber biosynthesis. In this chapter, we report on the current information as to the regulation of both HMGS and HMGR and their effect on rubber biosynthesis in H. brasiliensis. Hevea HMGS is encoded by a small gene family consisting of hmgs-1 and hmgs-2. The available information concerning the nature of the gene(s) encoding HMGS is also summarized. Enzyme activity and mRNA transcripts were mainly found in tissues with more laticifers, the sites of rubber biosynthesis. In latex of the high-yielding rubber clone, hmgs mRNA levels and enzyme activity were significantly higher than in the latex of the low-yield variety. Furthermore, the mRNA transcripts and enzyme activity in latex were higher at night than daytime, which is reflected by the dry rubber content. Ethephon treatment, which is known to increase the latex yield, had a direct effect on both hmgs mRNA transcripts and enzyme activity. The hmgs mRNA levels and dried rubber content per tapping from intra­clone rubber trees were also shown to be highly correlated. HMG-CoA acts as a substrate for HMGR to form mevalonate, which is further converted to isoprenoid compounds as well as natural rubber. Three genes are known to encode HMGR in H. brasiliensis, namely, hmgr-1, hmgr-2, and hmgr-3, and hmgr-1 is likely to be involved in rubber biosynthesis. The hmgr-1 mRNA level was well correlated with dried rubber content, similar to those observed in the case of hmgs gene expression.

These findings clearly indicated that both HMGS and HMGR enzyme activities are involved in early steps of rubber biosynthesis in H. brasiliensis at the level of their gene expression. The two enzymes possibly function in concert in response to the supply of substrate for rubber biosynthesis, similar to the synthesis of cholesterol in animals.

Keywords

HMG-CoA reductase HMC-CoA synthase Acetoacetyl-CoA Bacterial ACP synthase III (family) Rubber biosynthesis Hevea brasiliensis cis-1,4-Polyisoprene Laticifers Latex C-serum High rubber yield clones 

References

  1. Alam A, Britton G, Powls R et al (1991) Aspects related to 3-hydroxy-3-methylglutaryl-CoA synthesis in higher plants. Biochem Soc Trans 19:164–168Google Scholar
  2. Alex D, Bach TJ, Chye ML (2000) Expression of Brassica juncea 3-hydroxy-3-methylglutaryl-CoA synthase is developmentally regulated and stress-repressive. Plant J 22:414–426CrossRefGoogle Scholar
  3. Ayté J, Gil-Gómez G, Haro D et al (1990a) Rat mitochondrial and cytosolic 3-hydroxy-3-methylglutaryl-CoA synthase are encoded by two different genes. Proc Natl Acad Sci USA 87:3874–3878PubMedCrossRefGoogle Scholar
  4. Ayté J, Gil-Gómez G, Hegardt FG (1990b) Nucleotide sequence of a rat liver cDNA encoding the cytosolic 3-hydroxy-3-methylglutaryl coenzyme A synthase. Nucleic Acids Res 18:3642–3642PubMedCrossRefGoogle Scholar
  5. Bach TJ, Rogers DH, Rudney H (1986) Detergent-solubilization, purification, and characterization of membrane-bound 3-hydroxy-3-methylglutaryl coenzyme A reductase from radish seedlings. Eur J Biochem 154:103–111PubMedCrossRefGoogle Scholar
  6. Bach TJ, Raudot V, Vollack K-U et al (1994) Further studies on the enzymatic conversion of acetyl-coenzyme A into 3-hydroxy-3-methylglutaryl-coenzyme A in radish. Plant Physiol Biochem 32:775–783Google Scholar
  7. Balasubramaniam S, Goldstein JL, Brown MS (1977) Regulation of cholesterol synthesis in rat adrenal gland through coordinate control of 3-hydroxy-3-methylglutaryl-CoA synthase and reductase activity. Proc Natl Acad Sci USA 74:1421–1425PubMedCrossRefGoogle Scholar
  8. Brown WE, Rodwell VW (1980) Hydroxymethylglutaryl CoA reductase. In: Jeffery J (ed) Dehydrogenases requiring nicotinamide coenzymes. Birkhäuser Verlag, BerlinGoogle Scholar
  9. Chow K-S, Wan K-L, Isa MNM, Bahari A, Tan S-H, Harikrishna K, Yeang H-Y (2007) Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex. J Exp Bot 58:2429–2440PubMedCrossRefGoogle Scholar
  10. Chun KY, Vinarov DA, Zajicek J et al (2000) 3-Hydroxy-3-methylglutaryl-CoA synthase: a role for glutamate-95 in general acid/base catalysis of C–C bond formation. J Biol Chem 275:17946–17953PubMedCrossRefGoogle Scholar
  11. Chye ML, Kush A, Tan CT et al (1991) Characterization of cDNA and genomic clones encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from Hevea brasiliensis. Plant Mol Biol 19:562–577Google Scholar
  12. Chye ML, Tan CT, Chua NH (1992) Three genes encode 3-hydroxy-3-methylglutaryl coenzyme A reductase in Hevea brasiliensis: hmg1 and hmg2 are differentially expressed. Plant Mol Biol 19:473–484PubMedCrossRefGoogle Scholar
  13. Clinkenbeard KD, Reed WD, Mooney RD et al (1975a) Intracellular localization of the 3-hydroxy-3-methylglutaryl coenzyme A cycle enzymes in liver. J Biol Chem 250:3108–3116PubMedGoogle Scholar
  14. Clinkenbeard KD, Sugiyama T, Reed WD et al (1975b) Cytoplasmic 3-hydroxy-3-methylglutaryl coenzyme A synthase from liver: purification, properties and role in cholesterol synthesis. J Biol Chem 250:3124–3135Google Scholar
  15. Coupé M, Chrestin H (1989) Physiochemical and biochemical mechanisms of hormonal (ethylene) stimulation. In: Auzac JD, Jacob JL, Chrestin H (eds) Physiology of rubber tree latex. CRC Press, Boca RatonGoogle Scholar
  16. Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430PubMedCrossRefGoogle Scholar
  17. Hemmerlin A, Hoeffler JF, Meyer O et al (2003) Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem 278:26666–26676PubMedCrossRefGoogle Scholar
  18. Hepper CM, Audley BG (1969) The biosynthesis of rubber from β-Hydroxy-β- methylglutaryl coenzyme A in Hevea brasiliensis latex. Biochem J 114:379–386PubMedGoogle Scholar
  19. Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277:45188–45194PubMedCrossRefGoogle Scholar
  20. Lange BM, Rujan T, Martin W et al (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci USA 97:13172–13177PubMedCrossRefGoogle Scholar
  21. Laule O, Fürholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871PubMedCrossRefGoogle Scholar
  22. Lichtenthaler HK, Rohmer M, Schwender J (1997a) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652CrossRefGoogle Scholar
  23. Lichtenthaler HK, Schwender J, Disch A et al (1997b) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett 400:271–274PubMedCrossRefGoogle Scholar
  24. Lynen F (1969) Biochemical problems of rubber synthesis. J Rubb Res Inst Malaya 21:389–406Google Scholar
  25. Mandel MA, Feldmann KA, Herrera-Estrella L et al (1996) A novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9:649–658PubMedCrossRefGoogle Scholar
  26. Misra I, Miziorko HM (1996) Evidence for the interaction of avian 3-hydroxy-3 methylglutaryl-CoA synthase histidine-246 with acetoacetyl-CoA. Biochemistry 35:9610–9616PubMedCrossRefGoogle Scholar
  27. Misra I, Narasimhan C, Miziorko HM (1993) Avian 3-hydroxy-3-methylglutaryl-CoA synthase, characterization of a recombinant cholesterogenic isozymes and demonstration of the requirement for a sulfhydryl functionality in formation of the acetyl-S-enzyme reaction intermediate. J Biol Chem 268:12129–12135PubMedGoogle Scholar
  28. Misra I, Wang CZ, Miziorko HM (2003) The influence of conserved aromatic residue in 3-hydroxy-3-methyl­glutaryl-CoA synthase. J Biol Chem 278:26443–26449PubMedCrossRefGoogle Scholar
  29. Miziorko HM, Clinkenbeard KD, Reed WD et al (1975) 3-Hydroxy-3-methylglutaryl-CoA synthase. J Biol Chem 250:5768–5773PubMedGoogle Scholar
  30. Miziorko HM, Kramer PR, Kulkoski JA (1982) S-(3-Oxobutyl)coenzymeA. Interaction with acetoacetyl coenzyme A utilizing enzymes. J Biol Chem 257: 2842–2847PubMedGoogle Scholar
  31. Montamat F, Guilloton M, Karst F et al (1995) Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl-CoA synthase. Gene 167:197–201PubMedCrossRefGoogle Scholar
  32. Nagegowda DA, Bach TJ, Chye ML (2004) Brassica juncea 3-hydroxy-3-methylglutaryl (HMG)-CoA synthase 1: expression and characterization of recombinant wild-type and mutant enzymes. Biochem J 383: 517–527PubMedCrossRefGoogle Scholar
  33. Pojer F, Ferrer JL, Richard SB, Nagegowda DA, Chye ML, Bach TJ, Noel JP (2006) Structural basis for the design of potent and species-specific inhibitors of 3-hydroxy-3-methylglutaryl CoA synthases. Proc Natl Acad Sci USA 103:11491–11496PubMedCrossRefGoogle Scholar
  34. Price AC, Choi K-H, Health RJ et al (2001) Inhibition of β-ketoacyl-acyl carrier protein synthases by thiolactomycin and cerulenin. Structure and mechanism. J Biol Chem 276:6551–6559PubMedCrossRefGoogle Scholar
  35. Priya P, Venkatachalam P, Thulaseedharam A (2007) Differential expression pattern of rubber elongation factor (REF) mRNA transcripts from high and low yielding clones of rubber tree (Hevea brasiliensis Muell. Arg.). Plant Cell Rep 26:1833–1838PubMedCrossRefGoogle Scholar
  36. Pujade-Renaud V, Clement A, Perrot-Rechenmann C et al (1994) Ethylene-induced increase in glutamine synthetase activity and mRNA levels in Hevea brasiliensis latex cells. Plant Physiol 105:127–132Google Scholar
  37. Pujade-Renaud V, Clement A, Perrot-Rechenmann C et al (1997) Ethylene-induced increase in glutamine synthetase activity and mRNA levels in Hevea brasiliensis latex cells. Plant Physiol 105:127–132Google Scholar
  38. Qiu X, Janson CA, Konstantinidis AK et al (1999) Crystal structure of β-ketoacyl-acyl carrier protein synthase III: a key condensing enzyme in bacterial fatty acid biosynthesis. J Biol Chem 274:36465–36471PubMedCrossRefGoogle Scholar
  39. Reddy AR, Das VSR (1986) Partial purification and characterization of 3-hydroxy-3-methylglutaryl coenzyme A reductase from the leaves of guayule (Parthenium argentatum). Phytochemistry 25:2471–2474CrossRefGoogle Scholar
  40. Rogers DH, Panini SR, Rudney H (1983) Properties of HMG CoA reductase and its mechanism of action. In: Sabine JR (ed) 3-Hydroxy-3-methylglutaryl coenzyme A reductase. CRC Press, Boca RatonGoogle Scholar
  41. Royo T, Ayté J, Albericio FE et al (1991) Diurnal rhythm of rat liver cytosolic 3-hydroxy-3-methylglutaryl-CoA synthase. Biochem J 280:61–64PubMedGoogle Scholar
  42. Scarsdale JN, Kazanina G, He X et al (2001) Crystal structure of the Mycobacterium tuberculosis β-ketoacylacyl carrier protein synthase III. J Biol Chem 276:20516–20522PubMedCrossRefGoogle Scholar
  43. Schaller H, Grausem B, Benveniste P et al (1995) Expression of the Hevea brasiliensis (H.B.K.) Muell. Arg. 3-methylglutaryl-CoA reductase1 in tobacco results in sterol overproduction. Plant Physiol 109:761–770PubMedGoogle Scholar
  44. Seetang-Nun Y, Sharkey TD, Suvachittanont W (2008) Molecular cloning and characterization of two cDNAs encoding 1-deoxy-d-xylulose 5-phosphate reducto­isomerase from Hevea brasiliensis. Plant Physiol 165: 991–1002CrossRefGoogle Scholar
  45. Shah SN (1982) Cytosolic 3-hydroxy-3-methyglutaryl coenzyme A synthase in rat brain: properties and developmental change. Neurochem Res 7:1359–1366PubMedCrossRefGoogle Scholar
  46. Sipat AB (1982) Hydroxymethylglutaryl CoA reductase NADPH (EC 1.1.1.34) in the latex of Hevea brasiliensis. Phytochemistry 21:2613–2618CrossRefGoogle Scholar
  47. Sirinupong N, Suwanmanee P, Doolittle RR et al (2005) Molecular cloning of a new cDNA and expression of 3-hydroxy-3-methylglutaryl-CoA synthase gene from Hevea brasiliensis. Planta 221:502–512PubMedCrossRefGoogle Scholar
  48. Steinbüchel A (2003) Production of rubber-like polymers by microorganisms. Curr Opin Microbiol 6:261–270PubMedCrossRefGoogle Scholar
  49. Sutherlin A, Hedl M, Sanchez-Neri B et al (2002) Enterococcus faecalis 3-hydroxy-3-methylglutaryl-CoA synthase, an enzyme of isopentenyl diphosphate biosynthesis. J Bacteriol 184:4065–4070PubMedCrossRefGoogle Scholar
  50. Suvachittanont W, Wititsuwannakul R (1995) 3-Hydroxy-3-methylglutaryl coenzyme A synthase in Hevea brasiliensis. Phytochemistry 40:757–761CrossRefGoogle Scholar
  51. Suwanmanee P, Suvachittanon W, Fincher GB (2002) Molecular cloning and sequencing of a cDNA encoding 3-hydroxy-3-methylglutaryl-CoA synthase from Hevea brasiliensis (HBK) Muell Arg. Sci Asia 28:29–36CrossRefGoogle Scholar
  52. Van der Heijden R, de Boer-Hlupa V, Verpoorte R et al (1994a) Enzymes involved in the metabolism of 3-hydroxy-3-methylglutaryl-coenzyme A in Catharanthus roseus. Plant Cell Tiss Org Cult 38:345–349CrossRefGoogle Scholar
  53. Van der Heijden R, Verpoorte R, Duine JA (1994b) Biosynthesis of 3-hydroxy-3-methylglutaryl coenzyme A in Catharanthus roseus: acetoacetyl-Co A thiolase and HMG-Co A synthase show similar chromatographic behavior. Plant Physiol Biochem 32:807–812Google Scholar
  54. Vollmer SH, Mende-Mueller LM, Miziorko HM (1988) Identification of the site of the acetyl-S-enzyme formation on avian liver mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase. Biochemistry 27:4288–4292PubMedCrossRefGoogle Scholar
  55. Wegener A, Gimbel W, Werner T et al (1997) Molecular cloning of ozone-inducible protein from Pinus sylvestris L. with high sequence similarity to vertebrate 3- hydroxy-3-methylglutaryl-CoA synthase. Biochem Biophys Acta 28:247–252Google Scholar
  56. Wititsuwannakul R (1986) Diurnal variation of HMG-CoA reductase in latex of Hevea brasiliensis. Experientia 42:45–46CrossRefGoogle Scholar
  57. Wititsuwannakul R, Wititsuwannakul D, Suwanmanee P (1990) 3-Hydroxy-3-methylglutaryl coenzyme A reductase from the latex of Hevea brasiliensis. Phytochemistry 29:1401–1403CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Pluang Suwanmanee
    • 1
  • Nualpun Sirinupong
    • 2
  • Wallie Suvachittanont
    • 3
  1. 1.Biology DepartmentThaksin UniversityMuang DistrictThailand
  2. 2.Biochemistry and Molecular BiologyWayne State University School of MedicineDetroitUSA
  3. 3.Biochemistry DepartmentPrince of Songkla UniversityHat YaiThailand

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